Founder cell configuration drives competitive outcome within colony biofilms

Abstract

Bacteria typically form dense communities called biofilms, where cells are embedded in a self-produced extracellular matrix. Competitive interactions between strains within the biofilm context are studied due to their potential applications in biological, medical, and industrial systems. Combining mathematical modelling with experimental assays, we reveal that the spatial structure and the competitive dynamics within biofilms are significantly affected by the location and density of founder cells. Using an isogenic pair of Bacillus subtilis strains, we show that the observed spatial structure and relative strain biomass in a mature biofilm can be mapped directly to the locations of founder cells. Moreover, we define a predictor of competitive outcome that accurately forecasts relative abundance of strains based solely on the founder cells’ access to free space. Consequently, we reveal that variability of competitive outcome in biofilms inoculated at low founder density is a natural consequence of the random positioning of founding cells in the inoculum. Extending our study to non-isogenic strain pairs of B. subtilis, we show that even for strains with different antagonistic strengths, a race for space remains the dominant mode of competition in biofilms inoculated at low founder densities. Our results highlight the importance of spatial dynamics on competitive interactions within biofilms and hence to related applications.

A theoretical framework for multi-species range expansion in spatially heterogeneous landscapes

“…The accuracy of these predictions is similar to that reported from the spatially homogeneous case for which an alternative prediction method was used (Eigentler et al 2021). The predictive power of the Voronoi index is time-invariant, even though both the Voronoi index V i (t) and the competitive outcome B i Ω (t) are dynamic quantities that evolve over time during range expansion (Fig.…”

“…We also note a sharp decrease in variability of competitive outcome if the number of initial patches is decreased to N = 2. This also occurs in spatially homogeneous environments and we refer to (Eigentler et al 2021) for an interpretation of this phenomenon. The reported trends and the observed ranges of competitive outcome are very similar to those reported from spatially homogeneous domains ( (Eigentler et al 2021) and Fig.…”

“…The representation of very low initial population densities requires a different approach; at such densities, individuals are not necessarily spread uniformly in space. For example, inoculation of low densities of bacterial cells initially leads to the formation of small, spatially segregated microcolonies (Eigentler et al 2021), and invasion of mammal species into previously unoccupied habitats typically originate from a small number of individuals (Campbell et al 2012;Middleton 1930). To represent this initial clustering in the model, each species is initially confined to a number of small patches within Ω 0 in which their density is set to carrying capacity.…”

“…To understand the precise dynamics of competitive mechanisms affecting range expansion, it is therefore key to first attain knowledge about the role of spatial dynamics, in particular those that lead to spatial segregation. In a previous paper, we investigated the role of competition for space between two biofilm-forming bacterial strains in the specific case of microbial range expansion on spatially homogeneous substrates (Eigentler et al 2021). In brief, we revealed that the initial population density has a significant impact on competitive outcome (defined to be the relative abundance of one focal species across the whole community).…”

“…By contrast, low initial population densities resulted in highly variable competitive outcomes. Furthermore, in (Eigentler et al 2021) we defined a predictive tool that could be used to determine competitive outcome based solely on the distribution of the initial population. In short, the method is as follows.…”